Genomic Analysis of a Highly Virulent NDM-1-Producing Escherichia coli ST162 Infecting a Pygmy Sperm Whale (Kogia breviceps) in South America

Abstract

Carbapenemase-producing Enterobacterales are rapidly spreading and adapting to different environments beyond hospital settings. During COVID-19 lockdown, a carbapenem-resistant NDM-1-positive <i>Escherichia coli</i> isolate (BA01 strain) was recovered from a pygmy sperm whale (<i>Kogia breviceps</i>), which was found stranded on the southern coast of Brazil. BA01 strain belonged to the global sequence type (ST) 162 and carried the <i>bla</i> _NDM-1, besides other medically important antimicrobial resistance genes. Additionally, genes associated with resistance to heavy metals, biocides, and glyphosate were also detected. Halophilic behavior (tolerance to > 10% NaCl) of BA01 strain was confirmed by tolerance tests of NaCl minimal inhibitory concentration, whereas halotolerance associated genes <i>katE</i> and <i>nhaA</i>, which encodes for catalase and Na⁺/H⁺ antiporter cytoplasmic membrane, respectively, were <i>in silico</i> confirmed. Phylogenomics clustered BA01 with poultry- and human-associated ST162 lineages circulating in European and Asian countries. Important virulence genes, including the <i>astA</i> (a gene encoding an enterotoxin associated with human and animal infections) were detected, whereas <i>in vivo</i> experiments using the <i>Galleria mellonella</i> infection model confirmed the virulent behavior of the BA01 strain. WHO critical priority carbapenemase-producing pathogens in coastal water are an emerging threat that deserves the urgent need to assess the role of the aquatic environment in its global epidemiology.